1. No category

Series
HIV and sex workers 2
Combination HIV prevention for female sex workers: what is
the evidence?
Linda-Gail Bekker, Leigh Johnson, Frances Cowan, Cheryl Overs, Donela Besada, Sharon Hillier, Willard Cates Jr
Sex work occurs in many forms and sex workers of all genders have been affected by HIV epidemics worldwide. The
determinants of HIV risk associated with sex work occur at several levels, including individual biological and
behavioural, dyadic and network, and community and social environmental levels. Evidence indicates that effective
HIV prevention packages for sex workers should include combinations of biomedical, behavioural, and structural
interventions tailored to local contexts, and be led and implemented by sex worker communities. A model simulation
based on the South African heterosexual epidemic suggests that condom promotion and distribution programmes in
South Africa have already reduced HIV incidence in sex workers and their clients by more than 70%. Under optimistic
model assumptions, oral pre-exposure prophylaxis together with test and treat programmes could further reduce HIV
incidence in South African sex workers and their clients by up to 40% over a 10-year period. Combining these
biomedical approaches with a prevention package, including behavioural and structural components as part of a
community-driven approach, will help to reduce HIV infection in sex workers in different settings worldwide.
Introduction
The HIV epidemic continues to have a profound effect on
female, male, and transgender sex workers.1–4 The median
worldwide estimates show that female sex workers (FSWs)
are 13·5 (95% CI 10·0–18·1) times more likely to be living
with HIV than other women,3 15% of female HIV
infections in 2011 were attributed to sex workers, with the
highest attributable fraction in sub-Saharan African
populations (17·8%).5 Substantial proportions of new
infections (10–32%) occurred as a result of sex work in
West African countries. In Uganda, Swaziland, and
Zambia, 7–11% of new infections could be due to sex work,
sex-worker clients, and clients’ regular partners.6 The
UNAIDS 2015 goal of zero infections and discrimination
will need effective HIV prevention strategies for those who
sell or barter for sex in every region.1,4
Sex work is diverse and occurs in various contexts
around the world. Although some women sell sex
through formal structures such as brothels or other
venues, others might work independently and solicit
clients directly in public places or via cell phone or
internet.7,8 Tailoring of an effective, safe HIV prevention
package for FSWs to account for the contexts in which
they work and the particular risks they face is needed.7
Here, we have focused on prevention interventions for
FSWs and have defined sex work as exchange of sex for
money or goods. Prevention options for men (Baral and
colleagues9) and transgender persons who sell sex (Poteat
and colleagues10) are reviewed in this Series. HIV
prevention for women is a continuing challenge, and is an
area where biology, physiology, gender dynamics, and
behaviour have made HIV prevention research
challenging, particularly in the subset of women who sell
sex. We assessed interventions in three categories:
biological, behavioural, and structural.11,12 Effective HIV
prevention approaches for FSWs exist but have not been
taken to scale or adequately resourced in most parts of the
world.13 Additionally, we explored complementary
strategies that can be added to a combination prevention
package tailored for FSWs. An existing ecological model14
was modified to visualise multi-level domains of HIV risk
for FSWs (figure 1). We present within these multi-level
risks the evidence for biological, behavioural, and
structural prevention interventions (table 1). In this model,
we recommend that social justice principles are fully
Published Online
July 22, 2014
http://dx.doi.org/10.1016/
S0140-6736(14)60974-0
This is the second in a Series of
seven papers about HIV and sex
workers
For a Lancet HIV and sex
workers Series infographic see
http://www.thelancet.com/
series/HIV-and-sex-workers/
infographic
The Desmond Tutu HIV Centre
(Prof L-G Bekker PhD), and
Centre for Infectious Disease
Epidemiology and Research
(L Johnson PhD), University of
Cape Town, Republic of South
Africa; Research Department of
Infection and Population
Health, University College
London, London, UK
(F Cowan MD); Centre for
Sexual Health and HIV/AIDS
Research (CeSHHAR)
Key messages
• Effective HIV prevention approaches for female sex workers exist but have not been
taken to scale or adequately resourced in most parts of the world.
• Prevention interventions should integrate principles of social justice and meaningfully
include sex workers in programme design and implementation.
• Existing and effective prevention interventions include condom promotion, sexually
transmitted infection prevention and treatment, HIV counselling and testing, genderbased violence prevention, and economic and community empowerment.
• Stigma and criminalisation form barriers to such interventions and a less punitive
more enabling legal and medical environment is required.
• Modelling suggests that condom promotion may have already reduced incidence in
sex workers and their clients by up to 70% in South Africa. Additional biomedical
interventions such as pre-exposure prophylaxis or treatment as prevention could
further reduce this by 40%.
• Both topical and oral pre-exposure prophylaxis have been proven to reduce HIV
incidence in high-risk men and women. However, its effectiveness in sex workers has
yet to be determined.
• Earlier initiation of antiretroviral therapy, with the requisite access to services is likely
to benefit the health of sex workers and reduce HIV incidence in their clients and
others sexual partners.
• New biomedical technologies must be additive to, and not replacements for, more
established prevention modalities. Interventions that combine behavioural,
biological, and structural factors have the potential to have the greatest effect on the
health of sex workers, their clients, and the wider population.
www.thelancet.com Published online July 22, 2014 http://dx.doi.org/10.1016/S0140-6736(14)60974-0
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Zimbabwe, Harare, Zimbabwe
(F Cowan); Michael Kirby Centre
for Public Health and Human
Rights, Melbourne, Australia
(C Overs BA); The Desmond
Tutu HIV Foundation, Cape
Town, Republic of South Africa
(D Besada MPH); Unversity of
Pittsburgh Department of
Obstetrics, Gynecology and
Reproductive Sciences,
Pittsburgh, PA, USA
(S Hillier PhD); and FHI 360,
Durham, NC, USA
(W Cates Jr MD)
Correspondence to:
Prof Linda-Gail Bekker,
The Desmond Tutu HIV Centre,
Faculty of Health Sciences,
University of Cape Town, Anzio
Road, Observatory, 7705
Republic of South Africa
[email protected]
Search strategy and selection criteria
The literature review focused on HIV prevention programmes and
interventions, and in particular those that focused on the female
sex worker (FSW) population. This review included observational
studies, randomised controlled trials, and consensus papers or
programme reports from organisations, when they were peer
reviewed. We undertook a targeted web-based search of reported
literature from select sites including WHO and the Joint UN
Programme on HIV AIDS (UNAIDS) to retrieve information
regarding new policy guidelines on FSWs and the latest evidence
regarding HIV prevention. Data from systematic reviews of HIV
prevention interventions both in the female population and
general population were included as often data and programmes
specifically addressing FSWs were scarce. The review was
restricted to articles and documents published in English since
1990, with a particular emphasis on newer publications
beginning in 2000. PubMed and Google Scholar were searched in
addition to hand searching the bibliographies of selected peerreviewed articles. Key words for the search criteria included “HIV
integrated into any package of combination approaches
and that FSWs are meaningfully included in all aspects of
programme design and implementation.11,14–16 The
prevention strategies enable FSWs to exert more control
over their ability to prevent HIV. In addition to reducing
infections in FSWs, these strategies will positively affect
networks, communities, and country epidemics in
different social, economic, and legal contexts.17 We
modelled the effect of one such combination prevention
package within the setting of the South African epidemic.
Structural, social justice,
and human rights
Biomedical ART
and non-ART
Behavioural
Level of risk
Stage of epidemic
Public policy
Community
Indicator
Prevalence and incidence
Criminalisation, punitive laws, human rights contexts
Community cohesiveness, sex-worker friendly services, voluntary counselling and testing,
antiretroviral (ART) access, community-based structures, drug use programmes
Network
Sexual and physical violence, injection drug user networks, shared sex clients, HIV prevalence,
HIV knowledge, gender-based violence
Individual
Unprotected anal and vaginal sex, multiple concurrent partners, substance misuse,
gender-based violence, economic factors
Prevention intervention as part of highly active combination prevention
Figure 1: Framework for combination prevention: levels of risk and prevention interventions
2
prevention”, “Female SWs”, “IDU”, “PREP”, “peer support
programmes”, “PEP” and “STI treatment”, “ART”, “community
participation”, “condom use”, “biomedical HIV prevention”.
Abstracts of retrieved articles were read and if they were pertinent
to the research question, full texts were then retrieved. Due to the
dearth of information specifically related to HIV prevention in the
FSW population, inclusion criteria were broad to ensure a
comprehensive understanding of HIV interventions available,
even if they had not necessarily been tested in the specific
population in question. As the fields of HIV prevention
interventions are rapidly changing, with studies underway, the
review was updated several times. Of the 2350 papers identified
in the search, 69 were included that gave a broad range of
interventions that have an effect on HIV prevention, either in the
FSW population or general population. Those that did not directly
measure HIV prevalence or incidence reduction but were reported
to have a reduction on other factors (eg, STI treatment) known to
be linked to HIV reduction were also included.
Historical perspectives
FSWs were a key affected population in the early decades
of the HIV epidemic.18 HIV research with sex workers
contributed to improved knowledge about host immunity
in settings of recurrent infections19 and vaginal mucosal
integrity during the first microbicides trials.20,21
Nonoxynol-9, a contraceptive product viewed as safe, was
reported to be unsafe in sex work due to frequency of use
and subsequent mucosal erosion.22
In Thailand, the 100% condom campaign was more
than condom distribution: community mobilisation,
education, condom availability, consistent and universal
use of condoms, sexually transmitted infection (STI)
tracing in clients, and follow-up in brothels.23 This
programme and subsequent programmes in Cambodia
and elsewhere in Asia, showed marked population-level
effects of interventions focused on safer sex practices in
sex venues, including increasing condom use in sex
workers and clients and reductions in other STIs in STI
clinic attendees.24 Although HIV incidence was not
directly measured in these programmes, ecological data
suggest that they had significant effects on the trajectories
of the Thai and Cambodian HIV epidemics.25 The
appropriateness and sustainability of top-down structural
interventions that did not stimulate community empowerment have been restricted over time and critiqued by the
sex-worker rights movement. However, efforts to integrate
the positive policy elements of these models with sexworker participation and leadership have been successful
in other settings such as in the Collective Commitment
(Compromiso Colectivo) intervention in the Dominican
Republic.26 Community-based combination prevention
programmes in southeast Asia, Africa, and South America
confirm that HIV can be controlled both within FSW
networks and associated communities.27–29
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Community empowerment: promotion of social cohesion and capital, inclusion,
and leadership skills
Risk level
Type of intervention
Evidence in
FSWs
2, 3, 4
Structural
Direct
Advocacy and community mobilization: policy, programme, and services
3, 4
Structural
Direct
Gender-based and police violence, stigma, and discrimination
2, 3, 4
Structural
Direct
Economic strengthening, supplemental income
1, 2
Structural
Some
Rights, legal, and protection services
1, 4
Structural
Direct
Voluntary testing and linkage to services
1
Biomedical, behavioural, structural
Direct
Condoms (male, female, and condom-compatible lubricant)
1, 2, 3, 4
Biomedical, behavioural
Direct
Sex worker friendly health services, including sexual and reproductive health services
1, 2, 3, 4
Biomedical, structural
Direct
PrEP services
1, 2, 3
Biomedical, behavioural
Indirect
PEP services
1, 2, 3
Biomedical, behavioural
Indirect
HIV care, ART services, including PMTCT
1, 2, 3, 5
Biomedical, behavioural
Direct
Harm reduction in FSW-WID
1, 2, 4
Biomedical, structural, behavioural
Direct
Behaviour change by peer education and community-based counselling
1, 2, 3
Behavioural
Direct
FSW=female sex worker. PrEP=pre-exposure prophylaxis. PEP=post-exposure prophylaxis. ART=antiretroviral therapy. PMTCT=prevention of mother-to-child transmission.
WID=who inject drugs.
Table 1: Possible HIV prevention interventions that are supported by direct or indirect evidence in FSWs and the risk level at which they operate
The first oral pre-exposure prophylaxis (PrEP) trials in
FSWs in Cambodia in 2004 and in Cameroon in 2005
were halted after participant disquiet about trial
provisions.30,31 This led to a code of Good Participatory
Practice Guidelines and a benchmark for community
engagement in large prevention trials.32 Recent
prevention efficacy trials have not specifically included or
excluded FSWs and so the safety and effectiveness of
these newer modalities for FSWs remains unproven.
Existing prevention strategies
Existing prevention strategies include behavioural and
structural approaches, and sexual and reproductive
health services, including condoms, counselling, testing,
and supportive linkage to care for newly diagnosed
FSWs. The most effective strategies have been within
community-based programmes, which have intervened
on the drivers of HIV transmission in FSWs including
condomless sex, STIs, gender-based violence, unsafe
working environments, and poor service usage due to
stigma and discrimination.2
Condom provision
Sex worker projects worldwide show the feasibility of
increasing condom use to decrease STI and HIV
acquisition.33–35 In Santo Domingo, Dominican Republic,
condom use and rejection of condomless sex increased
because of workshops and meetings with sex workers, sex
establishment owners and managers, and other employees,
to strengthen collective commitment to prevention,
particularly in supporting sex workers to use condoms
with partners. These gatherings also focused on issues of
trust and intimacy in condom use negotiation between sex
workers and regular paying and non-paying partners.36,37
Interventions such as motivational interviewing have
improved condom use and harm reduction in FSWs who
also inject drugs.38
Greater success in uptake and adoption of condoms
has been reported in sex-worker programmes than any
other affected population. The latest UNAIDS report
states that countries’ reported condom use at last
commercial sex was high and improving; 44 countries
reported higher median condom use at last sex in 2012
than in 2009 (85% vs 78%).1 Cost and access to condoms,
and condom carriage used as evidence of sex work by
police in some settings are examples of structural
barriers that can undermine an effective intervention.
Provision of water-based lubricant with condoms is also
recommended, although less is known about the
importance of the type of lubricant. Although the
evidence for the preventive effect of female condoms is
scarce, some studies have shown higher acceptability of
female condoms in FSWs than other women.39,40
Furthermore, improving access to and reducing cost of
female condoms and lubricant could increase overall
condom usage.40 Condomless sex can be more lucrative
for a FSW, resulting in greater risk-taking for financial
reasons. To counter this issue, the role of cash transfers
for HIV prevention in sex work is also being investigated.
Cash transfer could operate on at least two levels:
conditional on safer sex practices as contingency
management, or as a way to reduce economic
vulnerability thereby encouraging behaviours with social
benefits.41 In the Zomba cash-transfer trial in Malawi,
adolescent girls who received transfer money were less
likely to have older sexual partners and had less frequent
sex, resulting in lower rates of HIV infection.42 In the
RESPECT study, beneficiaries were given rewards every
4 months for remaining free of curable STIs.43 After
1 year, the study recorded a 25% drop in the incidence of
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STIs. A pilot study is underway to explore cash transfers
in male sex workers in Mexico.44
Control of STIs
Bacterial and viral STIs can increase the efficiency of HIV
transmission. Screening and treating FSWs for STIs
could reduce HIV infections, although efficacy has been
difficult to demonstrate.45 STI treatment might consist of
active case finding and individual case management or
periodic mass STI treatment (periodic presumptive
treatment) regardless of diagnosis. Some empirical,
uncontrolled, intervention studies in sex workers and
community-based randomised controlled trials in general
populations have been undertaken.45–51 Only one
community-based trial (the Mwanza Trial) done in East
Africa showed efficacy of individualised syndromic
management of STIs against sexual transmission of HIV
with a reduction of 38% in HIV incidence.47,51,52 More than
12 500 individuals in the region were recruited to this trial
and it was estimated there were about 1200 sex workers or
bar workers in Mwanza town at this time.52 Where the
burden of STIs is high, periodic presumptive treatment
of curable STIs has been effective at reducing STIs but
not HIV incidence in FSWs.53,54 WHO advises only
temporary use of periodic presumptive treatment51,54 and
periodic presumptive treatment has a greater effect on
STI control in places where other aspects of control are
poor and where FSWs have little access to preventive and
curative services. Screening for asymptomatic STIs in
FSWs can reduce STIs,54 but in settings where resources
are scarce this is often not feasible. Syndromic
management to reduce STI infection in FSW networks is
problematic as most STIs are asymptomatic. This
situation might be changing, however, as point-of-care
STI diagnostics become more available and affordable.55
Clinical trials have not confirmed that herpes simplex
virus (HSV) suppressive treatment would reduce the risk
of HIV acquisition in HSV2-infected, HIV-uninfected
women. No protective effect of acyclovir was reported,
although some benefit was seen in a subset of women
who took at least 90% of their antiviral doses.56,57 These
studies were undertook in general populations with no
specific enrolment of sex workers56 and in women who
worked in venues such as bars and cafes in Tanzania
where 26–61% of enrolled women reported recent sex in
exchange for money.57 Poor adherence to bi-daily pills
probably contributed to results. Similarly, for individuals
co-infected with HIV and HSV2, treatment with daily
acyclovir to suppress HSV2 did not reduce the risk of
transmission of HIV to their partners.58
HIV testing and counselling
HIV testing underlies the implementation of nearly all
other prevention approaches and serostatus knowledge
is needed to tailor services to individual needs. However,
mandatory testing could be counter-productive and
violates rights—FSWs should be able to access HIV
4
testing and counselling with the same privacy and
protection as anyone else. WHO recommends at least
annual voluntary testing for sex workers. In a review of
52 low-income and middle-income countries in 2010, the
median percentage of FSWs who had tested for HIV in
the last 12 months and knew their test results was 49%
with wide variation across countries.59 Rates of HIV
testing in sex workers throughout Africa are suboptimal
with only 4% of sex workers surveyed in Somalia in 2008
ever-tested.60 Similarly, in Zimbabwe in 2011, where HIV
prevalence in sex workers is about 50%, half of
HIV-positive FSWs were aware of their status, only
30–40% of those eligible were accessing antiretroviral
therapy (ART) and fewer than a quarter of those HIVnegative reported testing in the previous 6 months.61
Indications are that testing coverage in FSWs has
improved in the era of ART access.62–64 Barriers to testing
in FSWs are similar to those of the general population:
poor awareness of services, distance to facilities,
transportation costs, opportunity costs, time constraints,
and fear of a positive result with resultant discrimination
and loss of income.65–68 However, additional barriers
unique to FSWs include fear of authorities, linked to sex
work illegality, and confidentiality concerns, particularly
status disclosure to other FSWs or potential clients.69,70
Several successful interventions have increased HIV
counselling and testing in sex workers.71–75 Strengthened
peer support and a supportive network are associated
with the willingness of FSWs to engage in testing, care,
treatment initiation, and adherence.26,74,75 Even when
FSWs have access to health facilities, prejudice and poor
quality of care are crucial determinants of their
willingness to be tested.76,77 There are studies regarding
the importance of affordable, sex-worker-friendly clinics,
and their ability to attract and retain FSWs.78–81
Gender-based violence interventions
Violence against sex workers is not only widespread, but
is also perpetrated, legitimised, and accepted by many,
including law enforcement authorities, gatekeepers,
managers, clients, and intimate partners.82 It undermines
HIV prevention efforts and increases the vulnerability of
sex workers to HIV transmission in several ways. Rape,
forceful acceptance of condomless sex, sex with police to
avoid arrest, and violence related to illicit drugs all could
result in FSWs giving higher priority to their safety and
survival than less immediate concerns such as HIV
prevention.83 Interventions include sex-worker education
on rights, community mobilisation to respond to violence
and discrimination, practical warning systems in sexwork networks, sensitisation workshops with police and
law enforcement authorities, and advocacy at community
and policy level to promote human rights of sex workers.83
Some innovations include the sex-worker education
programme devised by the Sex Workers Education and
Advocacy Taskforce (SWEAT) in South Africa and the
venue–level interventions identified by sex workers in
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Vancouver, including in-room buzzers and corridor video
surveillance.84,85
Community empowerment
Meaningful involvement of sex-worker communities in
the design and implementation of prevention programmes is crucial. Community empowerment reduces
the vulnerability of sex workers by peer-led collective
action and self-help activities including education, health
services, and advocacy on issues such as violence and
Population
(median age)
Total number
(women and
transgender
women)
Partners PrEP (Kenya Heterosexual
4747 (2283)
and Uganda)
men and women
(systemic PrEP)98
serodiscordant
(36)
work conditions.86,87 Interventions in programmes such as
Empower Thailand include sustained engagement with
local sex workers to raise awareness about sex-worker
rights, the establishment of safe spaces, the formation of
collectives that define the services to be provided, and
outreach and advocacy.88 Community empowerment is
associated with reduction in HIV and STI prevalence and
increased condom use.89 Importantly, community
empowerment is feasible to implement and take to scale,
is highly acceptable to FSWs, and is safe.90 Participation of
Percentage
reporting at
baseline
Design and
intervention
Relative
reduction in HIV
incidence ITT
Incidence
reduction in
women and
transgender
women
Definition of sex
work or any
associated risk
behaviours at
baseline
1:1:1 Oral TDF,
TVD, placebo for
negative partner
TDF 67% (95% CI
44–81), TVD 75%
(55–87)
TDF 68%
(29–85), TVD
62% (19–82)
<10% at baseline
Sex work and
transactional sex not
asked; any sex with
outside partner in the
previous month
Comments
Sub-analysis done in highrisk women. In subgroups
of women with placebo
group HIV-1 incidence
>5·0%, efficacy estimates
64–84%105
TDF2 (Botswana)
(systemic PrEP)100
1200 (548)
Negative
heterosexual
men and women
(25)
1:1 Oral TVD,
placebo
62% (22–83)
49·4% (–21·7 to
80·8; p=0·107)
Sex work and
transactional sex not
asked; asked whether
>1 sexual partner in
the last month
<20% at baseline
The Bangkok
Tenofovir Study
(Thailand) (systemic
PrEP)99
Negative PWID, 2413 (489)
men and women
(31)
1:1 Oral TDF,
placebo
49% (10–72)
78·6%
(16·8–96·7;
p=0·03)
Asked whether any
casual or sex work
partners in the past
3 months; >1 partner
in the last 3 months
Baseline 38% overall No specific data on sex
(men twice as much work in participants for
stratified analysis
as women); <20%
overall
FEM-PrEP (Kenya,
South Africa,
Tanzania)
(systemic PrEP)103
Negative
women (24)
2120 (2120)
1:1 Oral TVD,
placebo
No reduction
No reduction
12·6% at baseline
Asked whether sex
exchanged for money
and gifts in the last 4
weeks
Global iPrEx (USA,
Men and
Brazil, Peru, Ecuador, transgender
Thailand, South
women (27)
Africa) (systemic
102
PrEP)
2499 (all
participants had
to be born male,
although 29
[1%] reported
their present
identity as
female)
1:1 Oral TVD,
placebo
44% (15–63;
p=0·005)
Not done
Asked whether any
transactional sex in
the last 6 months
41% at baseline
Qualitative work in those
who reported sex work
has been undertaken and
will be reported
VOICE (MTN 003)
Negative
(Uganda, Zimbabwe, women (25)
South Africa)
(systemic and topical
PrEP)101
5029 (5029)
(2010 assigned
to gel groups)
1:1:1 Oral TDF,
TVD, TDF gel,
placebo
No reduction
No reduction
Asked whether
money, material
goods, gifts, drugs, or
shelter were received
in exchange for
vaginal or anal sex in
the last year
6·1% at baseline
304 out of 4980
participants responded yes
to this question at baseline.
No separate analyses
undertaken as numbers in
each study group
considered too small
1:1 Vaginal TDF
gel coitally
dependent,
placebo
39% (6–60)
39% (6–60)
Asked whether
money ever received
in exchange for sex
1·9% at baseline
Sample too small to do
separate analysis
1:1 Immediate vs
delayed ART for
positive partner
96% in linked
sexual
transmissions
Gender
insignificant
predictor of
linked
transmission
Transactional sex and
sex work not asked;
asked whether >1
partner in the last
3 months
<5% reported at
baseline
11 out of 39 transmission
events occurred outside of
the enrolled dyad
CAPRISA 004
(KwaZula Natal,
South Africa)
(topical PrEP)97,104
Negative
women (24)
HPTN 052 (USA,
Brazil, Botswana,
Zimbabwe, Malawi,
Kenya, South Africa,
India, Thailand)
(TasP)105
Men and women 3526 (1962)
serodiscordant
couples (32)
889 (889)
No stratified analysis in
specific risk groups
No significant relationship
between transactional sex
and HIV incidence or good
adherence
In RCTs where sex work was not asked, alternative associated risk behaviours have been listed. PrEP=pre-exposure prophylaxis. TasP=treatment as prevention. ITT=intention to treat. TDF=tenofovir.
TVD=emtricitabine and tenofovir (Truvada). ART=antiretroviral therapy.
Table 2: Completed PrEP and TasP studies, and outcomes by gender and participation of sex workers (if any)
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FSWs—most famously illustrated by the Sonagachi
Project in Northern Kolkata, India—has documented
increased condom use and decreased HIV prevalence not
only in FSWs but also in bridge populations.29,91 The
Sonagachi Project invested substantial effort to define the
problem of HIV prevention as a community issue and to
align the short-term and long-term rewards for condom
use as being in the economic best interests of all
stakeholders and the sex workers.91 This programme and
others show that sex-worker health outcomes can be
enhanced when programmes encourage a sense of shared
identity and camaraderie in sex workers, and address
concerns beyond HIV and sexual health, including
violence, stigma, and discrimination.27–29 Genderresponsive economic strengthening activities including
vocational training, education, and micro-financing
within empowerment programmes could also give FSWs
control over vital economic resources, and reduce FSW
vulnerability to HIV.92
Prevention taken to scale
HIV prevention interventions can be successfully taken
to scale with potential to reduce HIV prevalence in FSWs.
One such programme is the Avahan programme,
launched in 2003 by The Bill & Melinda Gates Foundation
in six Indian states. The programme aimed to reduce
HIV transmission and the prevalence of STIs in
vulnerable high-risk populations, notably FSWs. It
promoted prevention education and services such as
condom promotion, STI management, behaviour change
communication, community mobilisation, and advocacy.93 An important aspect of the Avahan programme
has been its coverage, with an 80% target met within
5 years, resulting in demonstrable increases in condom
uptake, and decreases in STIs and HIV.28 An example of
scale-up from Africa is the Zimbabwean Sisters with a
Voice programme, which is also community
empowerment based, and is now present in 36 sites
around the country, although studies on the effect of this
programme are awaited.27 Effective scale-up needs
commitment and sustained resources.13
However, it is possible that along with sustained
resources, strategies that address determinants in
addition to those listed above could be needed for
maximum prevention effect.94,95 After the 100% Thai
Condom campaign, for example, HIV prevalence levelled
at about 10% in FSWs, ten times higher than the
prevalence in Thai women from the general population.3
New prevention strategies
Combining the previous more established approaches
with new, partially effective biomedical modalities is a
potential new approach. In the last 3 years biomedical
interventions that use antiretroviral drugs as prevention
have become important. Antiretroviral drugs can protect
uninfected individuals from acquiring infection (PrEP
and post-exposure prophylaxis [PEP]), and can reduce
infectiousness of infected partners (secondary prevention
or treatment as prevention (TasP). Pre-exposure and
post-exposure antiretroviral drugs can be provided either
as oral (systemic) tablets or vaginal or rectal (topical) gels
or rings known as microbicides.96 The application of
antiretroviral drugs for HIV prevention to FSW
populations remains to be proven.
PrEP
Seven randomised controlled trials have examined
antiretroviral drugs given to HIV-negative persons for
HIV prevention (table 2).97–103 In four clinical trials
including women from diverse geographical and risk
settings, PrEP reduced HIV acquisition by 39–75%.97–100
None specifically enrolled FSWs, however in three of the
trials,97,101,103 most of the women were unmarried, up to a
quarter had many partners, and between 1·9% and 12%
reported transactional sex at baseline. No significant
relationship between transactional sex and HIV
incidence or good adherence rate was noted in the FEMPrEP study (J Headley, FHI 360, personal communication). The only other study in which transactional sex
was reported was the Global iPrEx Study102 that included
men who have sex with men—although all participants
had to be born male, 29 (1%) reported their present
Drug detection in blood and vaginal samples from
non-seroconverters
HIV protection estimate as related to high adherence
Partners PrEP98 (systemic PrEP)
81%
86% (TDF), 90% (TVD), in patients with detectable levels
TDF2100 (systemic PrEP)
79%
78% excluding follow-up when patients had no PrEP refills
FEM-PrEP103 (systemic PrEP)
35–38% at a single visit, 26% at two consecutive visits
Too low to assess efficacy
Global iPrEx102 (systemic PrEP)
51%
92% (95% CI 40–99) (TVD)
The Bangkok Tenofovir Study99
(Thailand) (systemic PrEP)
66%
74% in participants with detectable drug levels
VOICE101 (systemic and topical PrEP)
CAPRISA 00497 (topical PrEP)
<30% of samples; about 50% of women had no detectable levels Too low to assess efficacy
>1000 ng/mL TDF in vaginal fluid protective
54% in the high adherers, >80% of sex acts covered with
gel use
PrEP=pre-exposure prophylaxis. TDF=tenofovir. TVD=emtricitabine and tenofovir (Truvada).
Table 3: Completed PrEP (oral and topical) studies and protection estimates relative to adherence
6
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identity as female (table 2). Due to limited representation,
no randomised controlled trials have specifically
undertaken an efficacy sub-analysis in sex workers.
Consequently, any application to sex work is based on
extrapolation from a general female population, and
product safety and the effect of the conditions associated
with the nature of sex work (eg, frequency of sex and
therefore the frequency of dosing of coitally dependent
agents) on PrEP effectiveness is unknown.
A strong dose–response relationship between
adherence to PrEP pill-taking or gel-use and HIV
protection was shown (table 3). No HIV protection was
reported in the two trials in which adherence to PrEP was
lowest.101,103 By contrast, in the Partners PrEP (discordant
couples) and iPrEx (MSM) studies, case-control analyses
suggested that those using PrEP consistently had greater
than 90% reduction in HIV risk.98,102 The Partners PrEP
study team undertook an analysis in higher risk
subgroups within the Partners PrEP Study, including
groups of higher risk women. High risk was defined by
criteria including viral load of partner, unprotected sex,
and younger age. In these subgroups, PrEP had consistently higher efficacy for HIV-1 protection.106,107
The most recent clinical trial of systemic PrEP included
drug users in Thailand99 and had 2413 participants (about
20% were female). Participants were asked to report
whether they had sexual intercourse with people other
than their live-in partner including casual or sex work.
This behaviour was reported in 38% of the participants
(fewer women than men) at baseline (table 2). The HIV
incidence reduction of 49% for those on PrEP is
important because FSWs who inject drugs are often the
most vulnerable (and marginalised) subgroup of FSWs.108
HIV prevalence in women engaging in both injection
drug use and sex work is higher than in the general FSW
population.109,110 Women had the best adherence in this
study. Combination prevention packages, including
harm reduction strategies and PrEP for FSWs who inject
drugs, are promising.111
In studies where adherence was greatest, the positive
findings support the biological effectiveness of PrEP for
preventing HIV acquisition,96 but the trials with negative
results suggest that PrEP was an unacceptable or
unfeasible mode of prevention for some women. The
reasons for this are unknown but some of the reported
adherence barriers might be relevant to FSWs, including
absence of support from family and partners. Whereas
the possible role of low-risk perception by women might
seem less relevant to FSWs, it is well known that
intimate partners could present an unanticipated risk to
FSWs, with data to show that FSWs are less likely to use
condoms consistently with intimate partners.112,113
Acceptability studies (of hypothetical prevention
products) have been done in FSWs and have shown
favourable outcomes, but have also raised some
concerns from sex workers, including STI risk, privacy,
and cost.114,115
Topical vaginal gel applied during sexual intercourse in
the CAPRISA 004 study was protective and levels of
protection correlated with adherence.97 About 20 (1·9% of
all trial participants) were self-reported sex workers in this
study (table 2), too small a number for subgroup analyses.
Coital application could suit women having intermittent
sexual intercourse better than the more regular encounters
that occur in sex work. Coital application might be an
appealing dosing strategy for sex work, because the gel
can also lubricate. The maximum frequency of application
that would be safe in this setting is still unknown. Host
biological factors could alter the activity of topical
biomedical interventions; an analysis of HIV risk in
women in CAPRISA 004 showed that despite adequate
levels of vaginal tenofovir, women with higher systemic or
mucosal immune activation, such as might occur with
STIs, were more likely to become infected with HIV than
women without evidence of activation.116,117 Studies in
Kenyan sex workers have shown that resistance to HIV
infection could be attributed to a balance of immune
quiescence and a focused innate antiviral response.118
Additionally, complex questions regarding adherence
and dual-protection remain. Demonstration projects that
can assess the real-world effect of PrEP in sex workers
beyond clinical trial settings are needed. This might
include addressing concerns surrounding uptake, such
as cost and side-effects, adherence barriers such as
detention and reluctance to carry pills that could be
stigmatising, and combining PrEP usage with condoms
or other behavioural measures. PrEP is probably an
important addition to HIV prevention in transgendered
Sex-work-related factors that could affect effectiveness of PrEP and use
(systemic and topical)
Biomedical
Host factors
Systemic or mucosal immune activation
Frequency of sex
Daily product vs intermittent product use
Type of sex
Trauma, erosions; willingness to use a gel for added lubrication
Concurrent STIs
Erosions, ulcers, immune activation
Behavioural
Adherence to pill taking
and product use
Willingness to carry pills and products; difficulty taking daily pills and products
Adherence to programme
Willingness to be frequently tested and attend services regularly
Condom use
Less consistent use
Risk perception
Motivation to use daily product
Alcohol and drug misuse
Effect on adherence
Structural
Detention
Inability to adhere to pills or programme
Access to product and pills
Acceptable access points
Cost
Access to free product and willingness to pay
Intimate partners
Transmitted resistance; consistent use
Client-related factors
Transmitted resistance; pressure for condomless sex
Manager-related factors
Pressure for condomless sex; mandatory use and denied use
PrEP=pre-exposure prophylaxis. STI=sexually transmitted infection.
Table 4: Factors associated with sex work that affect the effectiveness of PrEP
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Population
Design, product, and follow-up duration
Location
Timeline
Clinical trials
FACTS 001
2600 heterosexual women
Placebo RCT, 1% TDF gel, BAT 24
South Africa
Enrolling, 2015
ASPIRE
Heterosexual women
Placebo RCT, dapivirine vaginal ring
Zimbabawe, Malawi,
Uganda, South Africa
Fully enrolled, 2015
RING study
Heterosexual women
Placebo RCT, dapivirine vaginal ring
South Africa
Enrolling, 2016
FACTS 002
100 young women
(aged 16–17)
Safety and acceptability, 1% TDF vaginal gel,
BAT 24
South Africa
Under review
CHAMPS-SA PLUSPILLS PrEP
150 young men and women
(aged 15–19)
Open label TVD oral
South Africa
Under review
Partners PrEP (post-placebo phase)
4747 heterosexual HIV
serodiscordant couples
Randomised daily oral TDF vs TVD (unblended), Kenya, Uganda
follow-up 12 months
Fully enrolled
CDC 494/TDF2 open-label extension
1219 heterosexual men and
women
Open label TVD, 12 months follow-up
Botswana
Enrolling, results 2014
Partners Demonstration Project
1000 HIV serodiscordant
couples
Open label, daily TVD oral as bridge to treatment
in infected partner, follow-up 24 months
Kenya, Uganda
Enrolling, results 2014–15
CAPRISA 008
··
Open label, 1% TDF vaginal gel, BAT 24
South Africa
Results 2015
SAPPH-Ire FSW RCT
2800 FSWs
Open label, oral daily TVD
Zimbabwe
Enrolling
TAPS: Expanded use of ART for treatment and
prevention for female sex workers in South Africa
400 FSWs for PrEP, 300 FSWs
for ART
Open label, PrEP for negative FSWs and
immediate ART for FSWs living with HIV
South Africa
Enrolling
Follow-on and demonstration studies
RCT=randomised controlled trial. TVD=emtricitabine and tenofovir (Truvada). TDF=tenofovir. PrEP=pre-exposure prophylaxis. BAT 24=one dose before sex, one dose after sex, but no more than two doses in
24 h. FSW=female sex worker.
Table 5: Trials in progress and planned, and demonstration PrEP (oral and topical) projects in women and female sex workers
FSWs in which the HIV transmission probability per
sexual transaction is very high. Although PrEP as a usercontrolled method might provide personal protection
against HIV, STIs and unwanted pregnancy for FSWs
remain a risk, especially if there is no option for condoms.
The implications for other STIs and unintended
pregnancy due to condom migration should be guarded
against with the ancillary provision of information and
sexual and reproductive health services. PrEP could be a
potent additional choice for some FSWs, but not all. The
challenge is to find ways that FSWs can identify suitability
for themselves. In all clinical trials, condom usage
increased and STI diagnoses decreased during the study,
suggesting that PrEP could work synergistically with
other prevention modalities;96 however, public awareness
of PrEP could lead to increased demand for condomless
commercial sex. PrEP should be part of a combination
prevention package that is voluntary and includes
condom promotion.119 As PrEP is introduced in sexworker populations, community engagement, further
behavioural and social science research, and careful
programme monitoring and assessment will be needed.119
Important research areas are listed in table 4.
WHO and Centers for Disease Control and Prevention
(CDC) have offered early guidance and have called for
demonstration projects including all key affected
populations.120–122 A variety of open-label and demonstration projects in women are on-going or imminent
and a confirmatory vaginal gel study is underway at
present.123 Zimbabwe has approved a PrEP demonstration
project in FSWs, SAPPH-Ire, which commenced in 2014
8
and will be nested within the already well-established
Sisters with a Voice Program (table 5).
PEP
PEP is most commonly used for needle-stick incidents
and, increasingly, for sexual assault. Non-occupational
PEP for sexual prevention has not been scaled up
worldwide. Reasons for this include user reluctance (the
need to access care within 72 h and continue treatment
for 28 days, and the side-effects), and inadequate services
(the need for testing and scarcity of PEP starter packs on
demand).124 PEP is probably not scalable, practical, or
sustainable as a sole intervention for sex workers,
although it has a role in sexual assault and other episodes
of unanticipated condomless sex. In a study from Kenya,
PEP was well accepted by urban FSWs with greater than
10% requesting PEP at least once during the year after its
introduction. However, PEP use was not associated with
reduced HIV acquisition in this study.125
Earlier treatment
Earlier treatment of HIV-positive FSWs can improve
clinical outcomes and reduce transmission of HIV to
their HIV-negative sexual partners, including clients.126,127
HPTN 052, a randomised controlled trial in
serodiscordant couples, showed a 96% reduction in HIV
transmission from HIV-positive individuals, treated
earlier and virally suppressed, when compared with
those in whom treatment was deferred.105 Importantly,
11 (28%) of 39 infections occurred as a result of
relationships outside of the treatment dyad. This study
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Modelling HIV prevention strategies: network
level effect
The interventions described here have proven or
plausible potential to protect the individual FSW, but the
effect of these interventions at a network or community
level depends on the local epidemic and setting.17 To
assess the probable effect of some of these newer HIV
prevention strategies for FSWs, we developed a
mathematical model applied to South Africa. South
Africa has a severe HIV epidemic that is generalised and
driven mostly by heterosexual sex. Our objectives were to
gauge the extent to which commercial sex drives
heterosexual HIV transmission; the effect of past
changes in condom use on HIV incidence in FSWs and
their clients; and the potential future effect of promoting
oral or topical PrEP, and earlier ART to FSWs in
South Africa.
The model (described in the appendix) stratifies the
population by age, sex, marital status, male circumcision
status, and sexual risk behaviour. HIV-infected adults
not on ART were divided into four CD4 groups further
stratified by knowledge of HIV status. The probability of
HIV transmission per sex act depended on the HIV
disease stage of the infected partner, the sex and
circumcision status of the uninfected partner, and the
type of relationship (sex-worker client, short-term
non-marital, or long-term marital). Rates of HIV
transmission also depended on levels of condom usage,
which were assumed to depend on the type of
relationship. Rates of condom use were assumed to
have increased over time, partly due to condom
Mean
Proportion of men who visit sex workers
35%
Scaling factor for male rate of visiting sex workers137†‡
3·50
0·25
Relative rate of visiting sex workers in married men138
750
Annual number of clients per sex worker139–144
Annual rate of retirement from sex work141,142
0·33
Annual rate of PrEP uptake in sex worker114
0·30
SD*
··
1·50
··
··
0·10
0·10
Average PrEP effectiveness98,100,101,103
40%
24%
Reduction in condom use in women using PrEP145
10%
10%
0·30
Annual rate of microbicide uptake in sex workers97,146,147
0·10
Average microbicide effectiveness97,101
25%
13%
Reduction in condom use in women using microbicides145
10%
10%
5
Average time spent on PrEP and microbicides (years)141
··
ART uptake in women with CD4 >350 cells/μL148
60%
16%
Reduction in infectiousness after ART initiation105,149-152
80%
12%
*SDs are shown only for those parameters that are included in the uncertainty analysis. Gamma priors are used to
represent uncertainty around all parameters, except for those that are formatted as percentages (uncertainty is
represented using beta prior distributions). †Further details in the appendix. ‡Based on fitting model to sex worker
population size estimates.137 PrEP=pre-exposure prophylaxis. ART=antiretroviral therapy.
Table 6: Commercial sex assumptions
promotion programmes and partly due to reductions in
unprotected sex after HIV diagnosis. The model was
fitted to age-specific HIV prevalence data from South
African antenatal and household surveys, and recorded
mortality data.
The change in HIV incidence in FSWs and their
clients over the period from mid-2015 to mid-2025 was
assessed if new HIV prevention strategies were
promoted to FSWs, alone or in combination. HIV
prevention programmes include oral PrEP, topical PrEP
(microbicides), and early ART together with 6-monthly
HIV screening (a TasP strategy, in which all
70
See Online for appendix
Sex workers
Clients
60
Reduction in new infections (%)
did not enrol sex workers nor enquire about transactional
sex, however these data suggest that encouraging HIVpositive sex workers to voluntarily access effective,
comprehensive HIV services will improve personal
health prognosis and might protect clients from
acquiring HIV infection from sex workers (table 2).105,127–131
Reduced HIV transmission could have indirect
prevention benefits within sex-worker networks.
Available information on ART coverage, retention,
adherence, and viral suppression in FSWs is restricted to
only a few research settings in sub-Saharan Africa,
North America, and Asia. These data suggest that FSWs
can attain high levels of adherence and viral suppression,
at least in the short term and in research settings. Some
adherence concerns have been raised.132 Information on
long-term outcomes and retention pre-ART are
particularly sparse.133 FSWs might delay or be denied
access to health care for reasons of stigma, cost, and
victimisation, which can hinder adequate treatment
outcomes, antenatal care, prevention of vertical HIV
transmission during pregnancy,134 and the prevention of
continuing transmission to clients. HIV services,
including ART, that are acceptable, effective, and
accessible for all FSWs have well documented individual
and public health benefits.51,135,136
50
40
30
20
10
0
–10
VM
PrEP
Test and treat
VM and PrEP
VM and PrEP,
and test and treat
Figure 2: Percentage reduction in new HIV infections in sex workers and clients from 2015 to 2025
Percentage reductions in clients are calculated only for infections acquired during commercial sex (excluding
infections acquired from non-commercial sex partners). Box-and-whisker plots represent minimum,
25th percentile, median, 75th percentile, and maximum values from the 1000 parameter values in the uncertainty
analysis. PrEP=pre-exposure prophylaxis. VM=vaginal microbicide.
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A
0·70
0·60
0·40
0·30
0·20
PrEP uptake per annum
0·50
0·10
0
0
10
20
30
40
50
60
70
PrEP effectiveness (%)
80
90
100
B
90
80
60
50
40
Early ART uptake (%)
70
30
20
50
55
60
–10 to 0%
0 to 10%
65
70
75
80
85
Reduction in infectiousness (%)
10 to 20%
20 to 30%
90
95
100
30 to 40%
40 to 50%
Figure 3: Effect of uptake and efficacy on percentage reduction in new HIV
infections from 2015 to 2025
(A) Reduction in incidence in sex workers if only PrEP is provided to sex workers.
(B) Reduction in incidence in clients if test and treat interventions are
introduced in sex workers. Percentage reductions in clients are calculated only
for infections acquired during commercial sex (excluding infections acquired
from non-commercial sex partners). Contour plots represent the expected
reductions in new HIV infections at different uptake and efficacy levels.
PrEP=pre-exposure prophylaxis.
HIV-diagnosed sex workers were offered ART regardless
of their CD4 count). Because of the uncertainty regarding
rates of uptake, effectiveness, and risk compensation for
the different prevention methods, an uncertainty
analysis was done to assess the range of possible results.
The distributions chosen to represent the uncertainty
around each parameter are summarised in table 6;
1000 parameter combinations were randomly sampled
from these distributions using Latin hypercube
sampling.153 Assumed male rates of sex-worker contact
and female rates of retirement from sex work were also
included in the uncertainty analysis.
When fitted to South African data sources, our model
suggested that in 1990 HIV transmission between FSWs
and their clients accounted for 11% of heterosexual
transmission in South Africa (IQR 8–14%). By 2010, this
proportion had declined to 6% (IQR 5–8%). This was
because transmission in high-risk groups accounted for
10
a lower fraction of total transmission as the epidemic
became more generalised, and condom use in FSWs and
their clients increased more than in other relationship
types.154 Increases in condom use accounted for a 65%
reduction in the HIV incidence rate in clients in 2010
and a 76% reduction in HIV incidence rates in FSWs.
Further details regarding the proportion of heterosexual
transmission attributable to commercial sex and the
effect of past increases in condom use are described in
the appendix.
Oral and topical PrEP alone would have only a modest
effect on HIV incidence in FSWs (figure 2). However,
substantial variation occurs in the range of possible
outcomes, with the assumed annual rate of PrEP uptake
and PrEP effectiveness being the most important
determinants of the percentage reduction in sex-worker
HIV incidence over the 2015–25 period (figure 3A).
Under pessimistic assumptions, if effectiveness was low
(<10%) and sex workers using PrEP reduced their
condom use by more than 10%, the net effect on HIV
incidence in FSWs could be negative, although there
would still be a positive effect on HIV incidence in
clients if women using PrEP were tested regularly,
because earlier diagnosis would reduce transmission
potential. Under very optimistic assumptions
(effectiveness >95% and rate of PrEP uptake >0·65 per
person-year), PrEP could reduce HIV incidence in South
African sex workers by 40% or more over the 2015–25
period (figure 3A). Further uncertainty analysis is
presented in the appendix.
A TasP strategy in FSWs would have a moderate effect
on HIV incidence rates in clients (but little effect in
FSWs). It would reduce incidence in South African
clients by 23% (IQR 19–28%) over the 2015–25 period
(figure 2), which would provide an indirect prevention
benefit to FSWs. The estimated effect was particularly
sensitive to the assumed proportion of FSWs who chose
early ART after diagnosis (before meeting standard
eligibility criteria) and the assumed reduction in
infectiousness after ART initiation (figure 3B). One
reason why this intervention does not have a more
substantial effect is that rates of HIV testing and ART
initiation in South Africa are already high (the modelled
proportion of HIV-positive sex workers receiving ART in
2015 is 60% before the introduction of the TasP strategy);
if we assumed that no prevention or treatment strategies
were available in South Africa before the TasP strategy,
the predicted effect would be a 54% reduction in HIV
incidence in clients (IQR 50–58%), with reductions as
large as 70% if rates of early ART uptake and virological
suppression were high.
Combining a TasP strategy with the provision of oral
and topical PrEP, the model estimates a 25% reduction
in HIV incidence in clients (IQR 19–32%) and an 11%
reduction in HIV incidence in sex workers (IQR 7–15%)
(figure 2). Further discussion of the model results and
limitations are included in the appendix.
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Combination prevention for FSWs:
five intervention levels
Scale-up of potential interventions to mitigate HIV
acquisition and transmission by FSWs includes factors
other than the hierarchy of scientific evidence.
Acceptability in the FSW community, cost, logistics, and
potential side-effects are additional factors.155,156
The design of an FSW-tailored HIV prevention package
needs an approach that recognises all levels of risk, and
consists of biomedical, behavioural, and structural
interventions (figure 1). The epidemic context (risk
level 5) in which the sex work occurs is an important
determinant of HIV risk, and the importance of sexworker-focused interventions depends on this context.17
In South Africa we estimated that between 6% and 11%
of adult HIV transmission is attributable to sex work, but
in other regions where the HIV epidemic is more
concentrated, FSW-specific interventions might be more
important. For example, other models suggest that
providing a topical gel to FSWs would reduce HIV
incidence in the general population by only 9% in the
South African context, compared with 48% in Benin157
where sex work is estimated to account for more than
half of HIV infections in men.158 Previous modelling has
shown that FSW interventions probably have less effect
in mature epidemics than in early-stage epidemics.159,160
The effect of promoting PrEP to high-risk groups is
highly dependent on sexual mixing patterns in the
population and levels of heterogeneity in HIV risk.161 Our
simulations suggest that TasP interventions could have
less effect in settings where access to HIV testing and
ART is already high.2 Other modelling studies suggest
that a high background level of ART coverage will
probably increase the cost per HIV infection prevented
by PrEP.162 This implies that the benefit of promoting
new prevention methods to FSWs is dependent on
pre-existing levels of access to HIV prevention and
treatment. Knowing the local epidemic and thus tailoring
the response to it, is a fundamental step advocated by
UNAIDS and increasingly adopted by national
programmes.17 The need for continuing epidemiological
monitoring and specific FSW surveillance in each
country is essential.158
Any HIV prevention package must consider
environmental or policy factors (risk level 4) that define
the conditions in which sex is bought and sold.16 These
factors include the capacity of FSWs to choose and use
products to protect against STIs, unintended pregnancy,
HIV, and other infections. Other contextual factors
include the criminalisation of sex work, and policies that
govern the conduct of sex work, which define the ability
of FSWs to access safe work places and confidential
services. Local laws and policy, and cultural factors affect
the levels of discrimination associated with accessing
HIV services or selling sex while living with HIV. The
contrast between a legalised indoors environment (where
women can access appropriate occupational health
services and are safer from violence) and the illegal
street-based environment (where women experience
constant violence and have high rates of drug use and
health problems) is stark when considering what
interventions could operate at risk level 4. These factors
can be subject to rapid change in any one setting.
Improved working conditions, reduction in police
brutality, and empowerment of FSWs have been
described because of policy reform and decriminalisation
of commercial sex in New Zealand and are well described
in this Series.2,163,164
Community-based services and community advocacy,
engagement, and mobilisation of the sex work
community are essential (risk level 3). In conjunction
with strong civil society and peer initiatives, these can
reduce the stigma, discrimination, and marginalisation
of FSWs, which are themselves determinants of risk.
Participatory programmes that have behavioural and
structural effects such as those seen in Sonagachi,
Avahan, and other community-based programmes are
examples.27–29,165 Our model suggests that condom
distribution and HIV communication programmes have
already had a substantial effect on HIV transmission
between FSWs and their clients in South Africa. These
programmes in combination are estimated to have
reduced HIV incidence in FSWs by 76% and clients by
65% in 2010. Similar success could have been achieved
in other regions where levels of condom use are already
high. A model-based assessment of the Avahan
programme in southern India suggests that since it
began, increases in condom use have reduced new HIV
infections by 48–67%,165 and similar reductions have
been estimated when modelling the effect of Project
SIDA in Benin, which has promoted condoms and STI
screening in FSWs.158 In 2007, the median proportion of
FSWs who reported condom use with their last client
was high in all regions,166 suggesting that existing
interventions in other regions might already have had an
important effect on HIV incidence in FSWs and their
clients, although this effect cannot be quantified in some
settings due to scarce data on trends in condom use and
HIV prevalence.
Network level factors (risk level 2) operate within
social, sexual, and injection networks, and are poorly
understood in the context of FSWs. Modelling studies
have suggested that in some settings, prevention
programmes that reach regular clients and managers
could be important in reducing HIV incidence in FSWs,
particularly when the average time spent in commercial
sex is short.167 Additionally, effective interventions at this
level are particularly relevant to STIs and needle and
syringe safety. Compounding factors that apply at the
community and network level include ethnic origin,
migration, citizenship status, literacy, economic
security, marital status, drug use, social capital, and
education—all factors strongly associated with HIV
acquisition in FSWs.
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We have already described a number of biomedical and
behavioural interventions that reduce HIV risk at the
individual level (risk level 1). Biomedical interventions
under development such as longer-acting vaginal rings,
long-acting injectable PrEP, and products that combine
antiretroviral agents, contraceptives, or other anti-STI
medications could facilitate adherence and enhance the
prevention package available to FSWs in the future.
Rectal microbicides could be of importance in sex work
associated with anal sex. A source of uncertainty when
considering the potential effect of oral and topical PrEP
is the probable extent of risk compensation. Increased
unprotected sex is less likely to attenuate the protective
value of PrEP when individuals recognise their risk, want
to use PrEP, and are motivated to be adherent.168 Data
from the Partners PrEP trial show that after unblinding,
individuals receiving PrEP were marginally more likely
to have unprotected sex with individuals other than their
study partner.145 Some modelling studies have also raised
this concern.169–171 High-quality social and behavioural
preparedness research is needed to track trends in
condom use, and incidence of STIs and unwanted
pregnancies.172
Tailored combination prevention for FSWs should take
into account the type of sex work. Some of the modalities
might be easier to implement in specific settings (eg,
100% condom promotion initially had an effect in
establishment-based FSWs). Reaching the poorest and
most marginalised sex workers (eg, those who work on
the street or at truck stops) still presents formidable
challenges for the future.
Conclusions
Reducing HIV transmissions associated with sex work by
making sex work safer both for the workers themselves
and their clients are important components in achieving
prevention services for all. This review gives evidence of
an impressive array of already existing prevention
modalities that can be combined and applied to reduce
risk of HIV acquisition in FSW populations worldwide.
New biomedical technologies, including topical and oral
antiretroviral-based PrEP and earlier antiretroviral TasP,
must be additive to, and not replacements for, more
established prevention modalities.12,16 We also emphasise
the paucity of information on the effectiveness in FSWs,
particularly of the newer modalities. The Sonagachi29 and
Empower Thailand173 programmes have shown the
importance of community-led initiatives to ensure
increasing resources are directed at a transformative
change in behaviour. These include individual interventions such as condom use, and structural interventions
such as law reform, protective policing, and comprehensive
and voluntary services.164 High levels of coverage and
usage of services, and quality and sustainability, are critical
to maximise the effect.13,164,174–176 Inadequate financing for
FSW HIV prevention programming is a crucial reason
why HIV prevention coverage remains so low.
12
Notwithstanding sex workers’ disproportionate risk of
acquiring HIV, prevention programmes for sex workers
account for a meagre share of HIV prevention funding
worldwide.13,164 In most regions, national governments
have allocated few national resources to prevent HIV in
sex workers, with international donors funding most of
the HIV prevention efforts for this group.13 Our model
simulations suggest that condom promotion and
distribution programmes in South Africa have already
reduced HIV incidence in FSWs and their clients by more
than 70%. Expansion of voluntary, effective early treatment
together with PrEP could further reduce HIV incidence in
South African FSWs and their clients. Careful, consultative
addition of these approaches in tandem to a tailored
prevention package for sex workers that recognises and
supports safe workplaces and respectful communities will
go far in eliminating HIV infections, eradicating
discrimination, and ending AIDS deaths.
Contributors
L-GB had overall responsibility for the first draft, writing, design of
figures and tables, and general reviews. LJ performed the modelling, and
was responsible for the first draft of the modelling section, and general
review and contribution to the manuscript and literature search. FC
contributed to the first draft and general review of the manuscript,
including the literature search and response to reviewers. CO
contributed to the general review, editing of the manuscript, literature
search, and response to reviewers. DB performed the initial literature
search, updated the review, and contributed to the general review and
response to reviewers. SH contributed to the overall review and editing
of the manuscript, data collection, and response to reviewers. WC
contributed to the first draft and general review, including the literature
search and response to reviewers. All authors contributed to the overall
design and approach, and approved the final manuscript.
Declaration of interests
We declare no competing interests.
Acknowledgments
L-GB is supported in part by National Institute of Allergy and Infectious
Diseases (NIAID), National Institutes of Health (NIH), UCT CTU grant
2UM1AI069519-08. LJ received support from NIH (1R01AI094586-01)
and Hasso Plattner Foundation. SH received support from NIAID,
Microbicide Trials Network (1UM1AI068633). WC received support from
USAID Preventive Technologies Agreement (GHO-A-00-09-00016-00)
and NIAID, NIH HIV Prevention Trials Network (1U01A1068619-01).
This article and The Lancet Series on HIV and sex workers was
supported by grants to the Center for Public Health and Human Rights
at Johns Hopkins Bloomberg School of Public Health from The Bill &
Melinda Gates Foundation and from The United Nations Family
Planning Association (UNFPA).
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